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Harbor seal (Phoca vitulina concolor), the most abundant marine mammal in the Gulf of Maine and
mid-Atlantic region.
Introduction
Seals as Sentinels
arbor seals (Phoca vitulina) are widely distributed in the temperate near-shore waters of the
northern hemisphere and are important indicators of coastal contamination because they occupy
a high trophic level, are long-lived (35-40 years),
and accumulate high concentrations of persistent
organic pollutants (POPs) and mercury through the
food chain. Lipophilic (fat soluble) POPs including
PCBs, dioxins, and DDT build up in fatty tissues
such as blubber and have been shown to cause immune- and endocrine-disrupting effects in seals and
other marine wildlife (De Swart et al. 1994, De Guise
et al. 2001). Evidence amassed over three decades
suggests that these compounds have caused reproductive impairment, hormone abnormalities, and
population declines in seals inhabiting industrialized
regions of Europe, North America, and Asia. It is
widely believed that immunotoxic chemicals such as
PCBs and dioxins have played a role in the recurring distemper virus outbreaks and mass mortalities
reported among seals since the 1980s, by altering
the animals’ normal immune resistance to disease
(Dietz et al. 1989, Van Loveren et al. 2000, Harding
et al. 2002). Unlike POPs, mercury preferentially
accumulates in muscle and liver tissue, and at high
levels, may place young seals at risk for liver damage and immune and neurotoxic effects following
exposure in utero and through nursing (AMAP 1998,
Shaw 2002).
Dr. Susan Shaw and co-workers at the Marine Environmental Research Institute (MERI), Center for Marine
Studies, in Blue Hill, Maine, have been studying the impacts of environmental pollutants on seals in the Gulf of
Maine and along the mid-Atlantic coast since 2001 as
part of the Seals as Sentinels project. This project has
generated the first extensive data reported in 25 years
on levels and effects of toxic contaminants in northwestern Atlantic harbor seals (Phoca vitulina concolor).
H
Peter Ralston
How are seals, as top predators, impacted
by toxic contaminants in Casco Bay and the
Gulf of Maine?
At present, there are an estimated 99,340 harbor seals
inhabiting the northwestern Atlantic coast extending from
the Gulf of Maine southward to the coast of New Jersey
(Gilbert et al. 2005). Considered relatively non-migratory, harbor seals feed on a variety of fish including hake,
herring, alewife, haddock, redfish, and winter flounder in
coastal and estuarine environments and are exposed to
contaminated habitats and prey across their range. In the
southerly portion of the range, coastal urban development
has resulted in some of the densest concentrations of
human populations in North America, and environmental
pollution has been a concern at least since the 1950s.
Similar to European seals, the harbor seal population has
experienced a series of mass mortalities since the 1980s
(Geraci et al. 1982, Duignan et al. 1995). The most recent
event occurred in 2004 among harbor seals in southern
Maine where approximately 300 animals, primarily pups,
were found dead on beaches in and around Saco Bay.
The possible role of immunotoxic chemicals (e.g., PCBs,
dioxins) in these outbreaks is not clear.
Casco Bay Estuary Partnership
61
60
PCBs
µg/g lipid weight
50
DDTs
CHLs
40
30
20
10
0
Adult M
Adult F Yearling
Pup
Fetus
Figure 7-1: Major POPS (PCBs, DDT, CHLs) (µg/g, lipid wt) in harbor seal blubber by age class
Contaminant Levels in Seals
A total of 34 stranded harbor seals (Phoca vitulina concolor) and 3 gray seals (Halichoerus gryphus), primarily pups
and yearlings, were collected by MERI at locations along the coast from Mount Desert Island, Maine to Long Island,
New York between 1991 and 2001-2002. Seal blubber, liver, and kidney samples were analyzed for a wide range
of organic contaminants and metals. PCBs, DDT, and chlordane-related compounds (CHLs), chemicals which were
banned in the U.S. in the late 1970s, were the predominant organic compounds found in harbor seal tissues, reflecting the extreme persistence of these substances in the marine food chain. The highest concentrations were found in
the adult male harbor seals and pups, with mean PCBs of 55 and 54 µg/g, lipid weight (lw), respectively, followed by
the yearlings, adult females, and fetuses (see Figure 7-1). Gray seals tend to have lower levels of POPs than harbor
seals (PCBs 18-27 µg/g, lw) which is likely due to their pelagic migratory patterns and feeding habits.
Cynthia Stroud
The accumulation pattern in the harbor seals reflects an age-dependent increase in adult males, whereas females
lower their levels by transferring a proportion of their body burdens to pups (Addison and Brodie 1977). In phocid
(true or earless) seals, lipophilic POPs are transferred from maternal lipid stores to some extent during gestation but particularly during lactation, so that the body
burdens of PCBs and DDTs are often higher in pups
at weaning than in their mothers. Although MERI did
not examine mother-pup pairs, levels in pups were five
times higher than those in adult females. Compared
with the fetuses, pups had PCB burdens an order of
magnitude higher, reflecting the greater importance of
breast milk as an exposure route.
Harbor seal mother making first contact with newborn pup, mid-coast Maine.
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Toxic Pollution in Casco Bay: Sources and Impacts
Lactational transfer may also pose an increased toxic
risk to pups compared with that of adult exposure
through feeding. As the lactating seal does not feed,
the bulk of her circulatory lipids are derived from the
blubber layer rather than from lipid sources in her diet
(Addison and Brodie 1987). During the fasting period,
as the mother loses weight, the nursing pup may be
exposed to the more toxic PCBs mobilized from the
mother’s fat stores, as compared with lower chlorinated, relatively less toxic PCBs which, if the mother were
feeding, would be obtained from fish.
Persistent Organic Pollutants
Figure 7-2a shows mean concentrations of PCBs and DDTs in blubber of harbor seals (all ages) from different regions of the northwestern Atlantic. The animals from southern Maine were harbor seal pups and yearlings collected in Cape Elizabeth (Casco Bay), Saco, Wells and Kennebunk. Across the range, PCB concentrations in these
seals exceed the estimated threshold value of ~17µg PCB/g, lw (ppm) in blubber for adverse effects including
effects on immune and endocrine functions in the species (Kannan et al. 2000). Region-wide, the highest concentrations were found in the seals from Narragansett Bay/Long Island Sound, although this distribution undoubtedly
reflects the large effect of age class on body burdens.
27
34
14
-
13
60
Mid Maine Coast
Casco Bay
29
21
10
Massachusetts Bay
24
10
PCBs
Narragansett Bay
DDT
Long Island
Figure 7-2a: PCB and DDT concentrations (µg/g, lipid wt) in
blubber of NW Atlantic harbor seals
49
46
29
17
Maine Coast
68
Casco Bay
25
Massachusetts Bay
Narragansett Bay
Long Island
PCBs
DDT
Figure 7-2b: PCB and DDT concentrations (µg/g, lipid wt) in
blubber of harbor seal pups
Figure 7-2b shows the higher PCB and
DDT levels in harbor seal pups from
three regions—mid-coast Maine, southern Maine, and Massachusetts Bay. The
highest PCB concentrations (mean 67.5
µg/g, lw) were found in pups from Massachusetts Bay, whereas levels were
slightly lower (mean 46 and 49 µg/g, lw)
in pups from Casco Bay/southern Maine
and eastern Maine, respectively. In the
four pups from Casco Bay/southern Maine,
PCB concentrations were highly variable,
ranging from 11 to 110 µg/g, lw.
As is clear from Figures 7-2a and 7-2b,
harbor seals from the northwestern Atlantic have elevated tissue burdens of toxic
organic contaminants that place them at risk
for adverse health effects (Shaw et al. 2005).
This is especially true for the seal pups,
which may be vulnerable to health impacts
when concentrations are an order of magnitude lower (Shaw et al. 1999). In fact, the
levels of PCBs found in these pups were 18
times higher than the concentrations
(~3 µg/g, lw) associated with altered immune and endocrine function biomarkers
(indicators) in stranded, rehabilitated harbor
seal pups from the California coast (Shaw et
al. 1999).
One of these markers is the lymphocyte
proliferation assay. Lymphocytes are a type
of white blood cell—T and B cells—involved
in immune response to foreign substances.
The assay measures the ability of the circulating lymphocytes to respond to foreign
substances in vitro (i.e, in cell culture). This
assay is an important indicator of contaminant-induced alterations in nonspecific
immune function. A lowered proliferative response is indicative of an animal’s reduced
ability to resist infection by viruses and other
pathogens, while an enhanced response
may reflect autoimmune disease or cancer.
Recently, Levin et al. (2005) reported enhanced lymphocyte proliferative responses
in free-ranging harbor seals from British
Casco Bay Estuary Partnership
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Thyroid hormone levels and retinols (vitamin A) in plasma are important biomarkers of contaminant-induced
endocrine disruption. Adequate levels of thyroid hormones and vitamin A are critical to normal growth and
development, including development of the immune
system, the reproductive system, and the brain. Exposure to PCBs and related POPs can reduce hormone
and retinol levels in animals and humans by various
mechanisms such as competitive binding to receptors
on carrier proteins.
MERI
Columbia with mean PCB concentrations in blubber as
low as 2.5 g/g, lw. This is consistent with earlier findings
by Shaw et al. (2003) of PCB-dioxin-related immune
enhancement in free-ranging adult harbor seals from
the Gulf of Maine.
Week-old harbor seal pup rescued at Blue Hill Falls,
mid-coast Maine.
Mercury and Other Metals
Concentrations of mercury found in liver
of the adult harbor seals are shown in
Figure 7-3 (Shaw, unpublished data).
64
38
Seal liver and kidney samples were also
tested for arsenic, cadmium, chromium,
42
lead, silver, selenium, copper and zinc,
16
but these metals were not detected at
levels of concern. While hepatic (liver)
78
mercury levels in the younger seals
Maine Coast
were relatively low, concentrations in
adult seals (mean 64.8 µg/g, wet weight)
Casco Bay
42
exceed the threshold level of 60 µg/g,
ww, for liver damage in mammals (AMAP
1998). Elevated mercury levels are
known to be common in livers of marine
Massachusetts Bay
mammals, and seals have evolved biochemical mechanisms involving selenium to detoxify (demethylate) and store
Narragansett Bay
Mercury
mercury in the form of less toxic (divalent)
mercury-selenide complexes (Wagemann
Selenium
Long Island
et al. 2000). However, the ability to detoxify and store mercury may not be pres- Figure 7-3: Mercury and Selenium concentrations (µg/g, wet wt)
in liver of adult harbor seals
ent in newborn and young seals following
exposure to the mother’s burden in utero
and while nursing, thus, these young and
developing seals may be at risk for mercury-related neurotoxicity and other effects.
Temporal Trends
DDT and, to a lesser extent, PCB burdens in northwestern Atlantic harbor seals have declined from the very high
levels reported in the 1970s (Gaskin et al. 1973, Shaw et al. 2005). Between 1971 and 2001, DDT levels in harbor
seal blubber (all ages) decreased by ~82% while PCB levels decreased by ~66%. In the adult males and pups, a
smaller decline of ~45% in PCB levels was observed over this thirty year period. This is consistent with trends in
other industrialized areas where a more rapid decline of DDT was observed after these compounds were banned
(Kennish 1992), while PCBs are still being released from stockpiled residues (Tanabe 1988). In seals from the
highly polluted Baltic Sea, DDT levels have decreased by 72-85% since the 1970s, while PCB levels showed only
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Toxic Pollution in Casco Bay: Sources and Impacts
a minor decrease of 25% in females and no decrease in males (Nyman et al. 2002). A similar trend was observed
in most Arctic marine mammal populations (AMAP 2000).
To examine changes over the past decade, MERI compared contaminant levels in blubber of yearling harbor
seals collected in 1991 and 2001-2002 (Shaw et al. 2005). Due to the small sample size (n=3) of the 1991
samples, no conclusions could be drawn, but the data show only small decreases in absolute concentrations of
the major contaminant groups, PCBs, DDTs, and CHLs, in seal blubber over this ten-year period, suggesting an
equilibrium in environmental cycling of these POPs in the northwestern Atlantic.
Global Comparisons
The levels of PCBs and DDTs found in northwestern Atlantic harbor seals are at the upper middle of the contamination
spectrum on a global scale (see Figure 7-4). PCB concentrations in the adult males and pups (55 and 54 µg/g, lw) are
approaching the high levels reported in stranded seals from the polluted Baltic Sea, Wadden Sea, western Mediterranean, and Caspian Sea (Luckas et al. 1990, Borrell et al. 1997, Kajiwara et al. 2002), and are slightly higher than
levels reported in blubber of harbor seals from the the coasts of Denmark (Storr-Hansen and Spiid 1993), eastern
England (Law et al. 1989) and northern Ireland found during the 1988 morbillivirus epizootic (an epidemic among
animals) (Mitchell and Kennedy 1992). Compared with Pacific coast seals, PCB concentrations in the harbor seal
pups, including the four pups from Casco Bay/southern Maine, are three-fold higher than those reported in stranded
harbor seal pups from southern Puget Sound, Washington, an area considered relatively polluted (Shaw 1998, Hong
et al. 1996), and an order of magnitude higher than the levels reported in stranded harbor seal pups from the California coast (Shaw et al. 1999).
DDT concentrations in harbor seal pups sampled by MERI were similar to those of Baltic seals and western Mediterranean monk seals (Monachus monachus) (Luckas et al. 1990; Borrell et al. 1997), reflecting the widespread
production and application of DDT in these areas. However, DDT levels in the pups were an order of magnitude
lower than the extremely high concentrations found in Caspian seals (Phoca caspica) (Kajiwara et al. 2002), reflecting recent uses of this pesticide in the former USSR (Federov 1999).
NW Atlantic harbor seal (adult m)
NW Atlantic harbor seal (pup)
Puget Sound harbor seal (pup)
CA harbor seal (pup)
Baltic Sea harbor seal (all ages)
1
PCB
DDT
2
North America
2
3
Wadden Sea harbor seal (all ages)
3
N. Ireland harbor seal (all ages)
4
W. Mediterranean monk seal (adult m)
5
Caspian seal (all ages, m)
MERI Data
1
Europe & Asia
6
0
30
60
90
120
150
µg/g lipid weight
1 Shaw et al. 2005
2 Shaw 1998
3 Luckas et al. 1990
4 Mitchell & Kennedy 1992
5 Borrell et al. 1997
6 Kajiwara et al. 2002
Figure 7-4: PCB and DDT concentrations (µg/g, lipid wt) in pinnipeds from different regions
Casco Bay Estuary Partnership
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160
premature pupping (150 ppm)
ppm lipid weight
120
80
40
0
Infertility/reproductive impairment (85 ppm)
Immune suppression (17 ppm)
Reduced thyroid hormone, retinol (17 ppm)
Immune alteration in pups (2.5 ppm)
Casco Bay harbor seals
NW Atlantic harbor seals
Figure 7-5: PCB concentrations (ppm, lipid wt) in NW Atlantic harbor seals and
estimated threshold levels of effects in pinnipeds
Mercury levels in liver of the adult harbor seals (males
and females) were similar to those reported in adult
seals from other polluted areas including grey and
ringed seals (Phoca hispida) from the Baltic and harp
seals (Phagophilus groenlandicus) from the Greenland
Sea (Nyman et al. 2002; Fant et al. 2001; Brunborg et
al. 2005). Their mercury levels were two-fold higher
than the levels found in Greenland hooded seals (Crystophora cristata) (Brunborg et al. 2005) and an order
of magnitude higher that those of ringed seals from
Svalbard, Norway, (Fant et al. 2001). Much higher concentrations (mean 134-4250 µg/g, ww) were reported in
livers of dolphins from the Mediterranean Sea (Frodello
et al. 2000).
Cynthia Stroud
Toxic Impacts: Conclusions
Harbor seal with three-week old nursing pup
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Toxic Pollution in Casco Bay: Sources and Impacts
As shown in Figure 7-5, PCB burdens in harbor seals
from the northwestern Atlantic exceed the estimated
threshold level of 17µg PCB/g, lw in blubber for adverse
effects on immune function (Kannan et al. 2000), and fall
within the estimated threshold level of 25-77 µg PCB/g,
lw for reproductive effects in marine mammals (AMAP,
2000). PCB burdens in the pups, including those from
Casco Bay/southern Maine, are an order of magnitude
higher than the concentrations associated with reduced
immune responses and hormone levels in stranded
harbor seal pups from California (Shaw et al. 1999) and
with altered immune responses in free-ranging pups
from British Columbia (Levin et al. 2005). Moreover, in
a previous study MERI reported significant correlations
between dioxin-like compounds in plasma and altered
immune responses in free-ranging adult harbor seals
from the Gulf of Maine (Shaw et al. 2003).
Mercury concentrations found in liver of adult harbor seals exceed the estimated threshold level of 60 µg/g lw for liver
damage in mammals (AMAP 1998), suggesting that harbor seal pups may be exposed to harmful levels of mercury
during gestation and lactation. These observations, together with reports of at least two, and possibly three large-scale
outbreaks of viral disease among these seals since the 1980s, suggest that the population is currently at risk for contaminant-related health effects. Although the present study was limited by a small sample size distributed over a large
geographic area, the toxic impacts of the current POP and mercury body burdens in these seals would be expected to
be considerable, particularly among the pups, leading to developmental deficits and compromised immune resilience,
which in turn, may place them at risk for future disease outbreaks.
The data generated by the Seals As Sentinels project are the first extensive, region-wide data in 25 years on
levels and effects of toxic contaminants in harbor seals from the northwestern Atlantic. While levels of the legacy
POPs (PCBs, DDT) are slowly declining in marine biota, blubber concentrations in northwestern Atlantic harbor
seals declined only slightly over the ten-year period 1991-2001, suggesting that these compounds are at equilibrium
in the marine ecosystem. Moreover, thousands of new chemicals are being released every year, and we have
recently documented the presence of the widely used flame retardants polybrominated diphenyl ethers (PBDEs),
perfluorooctanesulfonate (PFOS), and related perfluorinated chemicals at relatively high concentrations in harbor
seal tissues (Shaw et al. 2006a,b). These compounds of emerging concern are now being studied for their capacity to biomagnify and provoke effects in marine mammals and humans.
In view of the past vulnerability of northwestern Atlantic harbor seals to viral outbreaks, there is a clear need for continued research on larger sample sizes to ascertain body burdens and toxic impacts of the complex mixtures of contaminants to which these seals are exposed.
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Toxic Pollution in Casco Bay: Sources and Impacts